Mitochondrial proliferation in the permanent vs. temporary cold: enzyme activities and mRNA levels in Antarctic and temperate zoarcid fish

Abstract

Adjustments in mitochondrial properties and capacities are crucial in acclimatization to seasonal cold and in evolutionary cold adaptation of marine ectotherms. Although long-term compensatory increments in aerobic capacity of fish tissues have frequently been described in response to cold, much less is known about transitional phases and gene expression patterns involved. We investigated the time course of adjustment to acute cold in liver of eurythermal eelpout Zoarces viviparus. Whereas citrate synthase (CS) activity rose progressively in liver, cytochrome c oxidase (COX) activity was not altered during cold acclimation. Species-specific RNA probes were used to determine mRNA levels. CS mRNA (nuclear encoded) displayed a delayed, transient increase in response to cold, such that transcript levels did not parallel the change in enzyme activity. The enzyme activities and mRNA levels in the confamilial Antarctic Pachycara brachycephalum indicate cold compensation of CS activity in this cold-adapted species. The ratio of CS and COX activities was elevated in acclimation and adaptation to cold, indicating enhanced citrate synthesis over respiratory chain capacities in cold-adapted liver mitochondria. This may support enhanced lipid synthesis typically found in cold. The ratio of enzyme activity and transcript levels differed largely between Z. viviparus populations from the Baltic and North Seas, indicating the influence of unidentified parameters other than temperature. Transcript levels may not be tightly correlated with enzyme activities during thermal adaptation and thereafter. The time course of the acclimation process indicates that regulation at the translational and posttranslational levels predominates in adjustment to moderate thermal challenges.

Aerobic mitochondrial capacities in Antarctic and temperate eelpout (Zoarcidae) subjected to warm versus cold acclimation

“…Cold compensated CS activities after calculation for total liver were also found by Kent et al (1988) and Lannig et al (2003), though it is somewhat unexpected that the slightly lower specific enzyme (CS and IDH) activities in liver mitochondria of cold compared to warm acclimated North Sea eelpout remained uncompensated for despite the higher mitochondrial protein content in Z. viviparus acclimated to 5°C. In contrast to the present findings, Lucassen et al (2003) found higher CS activity per g liver during cold acclimation (3.5°C) in North Sea eelpout, however, it might be that cold compensation of CS activities only starts when temperature falls below 5°C. Lucassen et al found no differences in hepatosomatic indices, whereas, in the present study, cold acclimation led to elevated I H in Z. viviparus.…”

“…Lucassen et al found no differences in hepatosomatic indices, whereas, in the present study, cold acclimation led to elevated I H in Z. viviparus. It may well be that longterm cold acclimation (10 months in this study versus 25 days in the study by Lucassen et al 2003) led to a down-regulation of specific CS capacities associated with an increase in I H .…”

Oxygen limited thermal tolerance in fish?

“…Thermal adaptation is linked to temperature dependent gene expression, for example of key aerobic enzymes, as seen during seasonal as well as latitudinal cold adaptation (e.g. Hardewig et al, 1999;Lucassen et al, 2003). Rearrangements of aerobic metabolism also occur with a shift to lipid accumulation and energy storage (cf.…”

Thermal sensitivity of cellular energy budgets in some Antarctic fish hepatocytes

“…Eventually, this even led to the loss of respiratory proteins in the white blooded Channichthyidae (Di Prisco 2000). The downside of this high degree of coldspecialisation was the development of cold-stenothermy, mirrored by increased mitochondrial densities at uncompensated capacities (Johnston et al 1998;D'Amico et al 2002;Lucassen et al 2003) combined with reductions in hematocrit (Egginton 1997b) and cardiovascular output (Egginton 1997a). Specialisation has thus forced some of these species to lead a less active, rather sluggish lifestyle.…”